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Journal of Endocrinological Investigation

, Volume 39, Issue 11, pp 1295–1301 | Cite as

Consumption of extra-virgin olive oil rich in phenolic compounds improves metabolic control in patients with type 2 diabetes mellitus: a possible involvement of reduced levels of circulating visfatin

  • C. SantangeloEmail author
  • C. Filesi
  • R. Varì
  • B. Scazzocchio
  • T. Filardi
  • V. Fogliano
  • M. D’Archivio
  • C. Giovannini
  • A. Lenzi
  • S. Morano
  • R. Masella
Original Article

Abstract

Aim

Phenolic compounds naturally contained in extra-virgin olive oil (EVOO) have demonstrated anti-inflammatory and antioxidant properties. The present study aimed at evaluating the effects of a polyphenol-rich extra-virgin olive oil (EVOO) (high-polyphenol EVOO, HP-EVOO) on the metabolic control and the production of specific pro-/anti-inflammatory adipokines in overweight patients with type 2 diabetes mellitus (T2D).

Methods

Eleven overweight T2D patients not in treatment with insulin were invited to follow their habitual diet for a total of 8 weeks. During the first 4 weeks (wash-out period), they were asked to consume refined olive oil (ROO, polyphenols not detectable) and then to replace ROO with HP-EVOO (25 mL/day, 577 mg of phenolic compounds/kg) for the remaining 4 weeks. Anthropometric parameters, fasting glycaemia, glycated haemoglobin (HbA1c), high-sensitive C-reactive protein, plasma lipid profile, liver function and serum levels of TNF-α, IL-6, adiponectin, visfatin and apelin were assessed at the end of each 4-week period.

Results

HP-EVOO consumption significantly reduced fasting plasma glucose (P = 0.023) and HbA1c (P = 0.039) levels as well as BMI (P = 0.012) and body weight (P = 0.012). HP-EVOO ingestion determined a reduction in serum level of aspartate aminotransferase (AST, P = 0.0056) and alanine aminotransferase (ALT, P = 0.024). Serum visfatin levels strongly decreased after HP-EVOO ingestion (P = 0.0021).

Conclusions

Daily consumption of polyphenol-rich EVOO might improve metabolic control and circulating inflammatory adipokines profile in overweight T2D patients.

Keywords

Type 2 diabetes mellitus Olive oil Polyphenols HbA1c Cytokines Visfatin 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving humans were in accordance with the ethical standards of the institution or practice at which the studies were conducted, and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Tuomilehto J, Lindstrom J, Eriksson JG et al (2001) Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N Engl J Med 344:1343–1350. doi: 10.1056/NEJM200105033441801 CrossRefPubMedGoogle Scholar
  2. 2.
    Khazrai YM, Defeudis G, Pozzilli P (2014) Effect of diet on type 2 diabetes mellitus: a review. Diabetes Metab Res Rev 30(Suppl 1):24–33. doi: 10.1002/dmrr.2515 CrossRefPubMedGoogle Scholar
  3. 3.
    Hirai S, Takahashi N, Goto T, Lin S, Uemura T, Yu R, Kawada T (2010) Functional food targeting the regulation of obesity-induced inflammatory responses and pathologies. Mediat Inflamm 2010:367838. doi: 10.1155/2010/367838 CrossRefGoogle Scholar
  4. 4.
    Bluher M (2014) Adipokines–removing road blocks to obesity and diabetes therapy. Mol Metab 3:230–240. doi: 10.1016/j.molmet.2014.01.005 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Chang YH, Chang DM, Lin KC, Shin SJ, Lee YJ (2011) Visfatin in overweight/obesity, type 2 diabetes mellitus, insulin resistance, metabolic syndrome and cardiovascular diseases: a meta-analysis and systemic review. Diabetes Metab Res Rev 27:515–527. doi: 10.1002/dmrr.1201 CrossRefPubMedGoogle Scholar
  6. 6.
    Bertrand C, Valet P, Castan-Laurell I (2015) Apelin and energy metabolism. Front Physiol 6:115. doi: 10.3389/fphys.2015.00115 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Georgoulis M, Kontogianni MD, Yiannakouris N (2014) Mediterranean diet and diabetes: prevention and treatment. Nutrients 6:1406–1423. doi: 10.3390/nu6041406 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Salas-Salvado J, Bullo M, Estruch R et al (2014) Prevention of diabetes with Mediterranean diets: a subgroup analysis of a randomized trial. Ann Intern Med 160:1–10. doi: 10.7326/M13-1725 CrossRefPubMedGoogle Scholar
  9. 9.
    Covas MI, de la Torre R, Fito M (2015) Virgin olive oil: a key food for cardiovascular risk protection. Br J Nutr 113(Suppl 2):S19–S28. doi: 10.1017/S0007114515000136 CrossRefPubMedGoogle Scholar
  10. 10.
    Cicerale S, Lucas L, Keast R (2010) Biological activities of phenolic compounds present in virgin olive oil. Int J Mol Sci 11:458–479. doi: 10.3390/ijms11020458 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Martin-Pelaez S, Covas MI, Fito M, Kusar A, Pravst I (2013) Health effects of olive oil polyphenols: recent advances and possibilities for the use of health claims. Mol Nutr Food Res 57:760–771. doi: 10.1002/mnfr.201200421 CrossRefPubMedGoogle Scholar
  12. 12.
    Cicerale S, Lucas LJ, Keast RS (2012) Antimicrobial, antioxidant and anti-inflammatory phenolic activities in extra virgin olive oil. Curr Opin Biotechnol 23:129–135. doi: 10.1016/j.copbio.2011.09.006 CrossRefPubMedGoogle Scholar
  13. 13.
    Santangelo C, Vari R, Scazzocchio B, Filesi C, Masella R (2014) Management of reproduction and pregnancy complications in maternal obesity: which role for dietary polyphenols? BioFactors 40:79–102. doi: 10.1002/biof.1126 CrossRefPubMedGoogle Scholar
  14. 14.
    Gimeno E, Castellote AI, Lamuela-Raventos RM, de la Torre-Boronat MC, Lopez-Sabater MC (2001) Rapid high-performance liquid chromatographic method for the simultaneous determination of retinol, alpha-tocopherol and beta-carotene in human plasma and low-density lipoproteins. J Chromatogr B Biomed Sci Appl 758:315–322CrossRefPubMedGoogle Scholar
  15. 15.
    Cavina G, Gallinella B, Porra R, Pecora P, Suraci C (1988) Carotenoids, retinoids and alpha-tocopherol in human serum: identification and determination by reversed-phase HPLC. J Pharm Biomed Anal 6:259–269CrossRefPubMedGoogle Scholar
  16. 16.
    Owen RW, Giacosa A, Hull WE, Haubner R, Wurtele G, Spiegelhalder B, Bartsch H (2000) Olive-oil consumption and health: the possible role of antioxidants. Lancet Oncol 1:107–112CrossRefPubMedGoogle Scholar
  17. 17.
    Suarez M, Valls RM, Romero MP, Macia A, Fernandez S, Giralt M, Sola R, Motilva MJ (2011) Bioavailability of phenols from a phenol-enriched olive oil. Br J Nutr 106:1691–1701. doi: 10.1017/S0007114511002200 CrossRefPubMedGoogle Scholar
  18. 18.
    Itsiopoulos C, Brazionis L, Kaimakamis M, Cameron M, Best JD, O’Dea K, Rowley K (2011) Can the Mediterranean diet lower HbA1c in type 2 diabetes? Results from a randomized cross-over study. Nutr Metab Cardiovasc Dis 21:740–747. doi: 10.1016/j.numecd.2010.03.005 CrossRefPubMedGoogle Scholar
  19. 19.
    Konstantinidou V, Covas MI, Munoz-Aguayo D et al (2010) In vivo nutrigenomic effects of virgin olive oil polyphenols within the frame of the Mediterranean diet: a randomized controlled trial. FASEB J 24:2546–2557. doi: 10.1096/fj.09-148452 CrossRefPubMedGoogle Scholar
  20. 20.
    Guasch-Ferre M, Hruby A, Salas-Salvado J, Martinez-Gonzalez MA, Sun Q, Willett WC, Hu FB (2015) Olive oil consumption and risk of type 2 diabetes in US women. Am J Clin Nutr 102:479–486. doi: 10.3945/ajcn.115.112029 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Esposito K, Giugliano D (2014) Mediterranean diet and type 2 diabetes. Diabetes Metab Res Rev 30(Suppl 1):34–40. doi: 10.1002/dmrr.2516 CrossRefPubMedGoogle Scholar
  22. 22.
    Khaw KT, Wareham N, Luben R, Bingham S, Oakes S, Welch A, Day N (2001) Glycated haemoglobin, diabetes, and mortality in men in Norfolk cohort of european prospective investigation of cancer and nutrition (EPIC-Norfolk). BMJ 322:15–18CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Esposito K, Maiorino MI, Di Palo C, Giugliano D, Campanian Postprandial Hyperglycemia Study G (2009) Adherence to a Mediterranean diet and glycaemic control in type 2 diabetes mellitus. Diabet Med 26:900–907. doi: 10.1111/j.1464-5491.2009.02798.x CrossRefPubMedGoogle Scholar
  24. 24.
    Petelin A, Bizjak M, Cernelic-Bizjak M, Jurdana M, Jakus T, Jenko-Praznikar Z (2014) Low-grade inflammation in overweight and obese adults is affected by weight loss program. J Endocrinol Investig 37:745–755. doi: 10.1007/s40618-014-0102-9 CrossRefGoogle Scholar
  25. 25.
    Schroder H, Marrugat J, Vila J, Covas MI, Elosua R (2004) Adherence to the traditional mediterranean diet is inversely associated with body mass index and obesity in a spanish population. J Nutr 134:3355–3361PubMedGoogle Scholar
  26. 26.
    Marrugat J, Covas MI, Fito M et al (2004) Effects of differing phenolic content in dietary olive oils on lipids and LDL oxidation: a randomized controlled trial. Eur J Nutr 43:140–147. doi: 10.1007/s00394-004-0452-8 CrossRefPubMedGoogle Scholar
  27. 27.
    Masella R, Giovannini C, Vari R, Di Benedetto R, Coni E, Volpe R, Fraone N, Bucci A (2001) Effects of dietary virgin olive oil phenols on low density lipoprotein oxidation in hyperlipidemic patients. Lipids 36:1195–1202CrossRefPubMedGoogle Scholar
  28. 28.
    Gimeno E, Fito M, Lamuela-Raventos RM, Castellote AI, Covas M, Farre M, de La Torre-Boronat MC, Lopez-Sabater MC (2002) Effect of ingestion of virgin olive oil on human low-density lipoprotein composition. Eur J Clin Nutr 56:114–120. doi: 10.1038/sj.ejcn.1601293 CrossRefPubMedGoogle Scholar
  29. 29.
    Farrell N, Norris G, Lee SG, Chun OK, Blesso CN (2015) Anthocyanin-rich black elderberry extract improves markers of HDL function and reduces aortic cholesterol in hyperlipidemic mice. Food Funct 6:1278–1287. doi: 10.1039/c4fo01036a CrossRefPubMedGoogle Scholar
  30. 30.
    Ali F, Jamil H, Anwar SS, Wajid N (2015) Characterization of lipid parameters in diabetic and non-diabetic atherosclerotic patients. J Geriatr Cardiol JGC 12:37–43. doi: 10.11909/j.issn.1671-5411.2015.01.005 PubMedGoogle Scholar
  31. 31.
    Ho CI, Chen JY, Chen SY, Tsai YW, Weng YM, Tsao YC, Li WC (2015) Relationship between TG/HDL-C ratio and metabolic syndrome risk factors with chronic kidney disease in healthy adult population. Clin Nutr 34:874–880. doi: 10.1016/j.clnu.2014.09.007 CrossRefPubMedGoogle Scholar
  32. 32.
    Fito M, Cladellas M, de la Torre R et al (2008) Anti-inflammatory effect of virgin olive oil in stable coronary disease patients: a randomized, crossover, controlled trial. Eur J Clin Nutr 62:570–574. doi: 10.1038/sj.ejcn.1602724 CrossRefPubMedGoogle Scholar
  33. 33.
    Urpi-Sarda M, Casas R, Chiva-Blanch G et al (2012) Virgin olive oil and nuts as key foods of the Mediterranean diet effects on inflammatory biomakers related to atherosclerosis. Pharmacol Res 65:577–583. doi: 10.1016/j.phrs.2012.03.006 CrossRefPubMedGoogle Scholar
  34. 34.
    Chang YC, Chang TJ, Lee WJ, Chuang LM (2010) The relationship of visfatin/pre-B-cell colony-enhancing factor/nicotinamide phosphoribosyltransferase in adipose tissue with inflammation, insulin resistance, and plasma lipids. Metabolism 59:93–99. doi: 10.1016/j.metabol.2009.07.011 CrossRefPubMedGoogle Scholar
  35. 35.
    Chen MP, Chung FM, Chang DM, Tsai JC, Huang HF, Shin SJ, Lee YJ (2006) Elevated plasma level of visfatin/pre-B cell colony-enhancing factor in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab 91:295–299. doi: 10.1210/jc.2005-1475 CrossRefPubMedGoogle Scholar
  36. 36.
    Filippatos TD, Derdemezis CS, Kiortsis DN, Tselepis AD, Elisaf MS (2007) Increased plasma levels of visfatin/pre-B cell colony-enhancing factor in obese and overweight patients with metabolic syndrome. J Endocrinol Invest 30:323–326CrossRefPubMedGoogle Scholar
  37. 37.
    Shaker O, El-Shehaby A, Zakaria A, Mostafa N, Talaat S, Katsiki N, Mikhailidis DP (2011) Plasma visfatin and retinol binding protein-4 levels in patients with type 2 diabetes mellitus and their relationship to adiposity and fatty liver. Clin Biochem 44:1457–1463. doi: 10.1016/j.clinbiochem.2011.08.1148 CrossRefPubMedGoogle Scholar
  38. 38.
    Dray C, Knauf C, Daviaud D et al (2008) Apelin stimulates glucose utilization in normal and obese insulin-resistant mice. Cell Metab 8:437–445. doi: 10.1016/j.cmet.2008.10.003 CrossRefPubMedGoogle Scholar
  39. 39.
    Cheng X, Cheng XS, Pang CC (2003) Venous dilator effect of apelin, an endogenous peptide ligand for the orphan APJ receptor, in conscious rats. Eur J Pharmacol 470:171–175CrossRefPubMedGoogle Scholar
  40. 40.
    Habchi M, Duvillard L, Cottet V et al (2014) Circulating apelin is increased in patients with type 1 or type 2 diabetes and is associated with better glycaemic control. Clin Endocrinol (Oxf) 81:696–701. doi: 10.1111/cen.12404 CrossRefGoogle Scholar
  41. 41.
    Kadoglou NP, Sailer N, Kapelouzou A, Lampropoulos S, Vitta I, Kostakis A, Liapis CD (2012) Effects of atorvastatin on apelin, visfatin (nampt), ghrelin and early carotid atherosclerosis in patients with type 2 diabetes. Acta Diabetol 49:269–276. doi: 10.1007/s00592-011-0310-0 CrossRefPubMedGoogle Scholar
  42. 42.
    Villegas R, Xiang YB, Elasy T et al (2011) Liver enzymes, type 2 diabetes, and metabolic syndrome in middle-aged, urban Chinese men. Metab Syndr Relat Disord 9:305–311. doi: 10.1089/met.2011.0016 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Kunutsor SK, Apekey TA, Walley J (2013) Liver aminotransferases and risk of incident type 2 diabetes: a systematic review and meta-analysis. Am J Epidemiol 178:159–171. doi: 10.1093/aje/kws469 CrossRefPubMedGoogle Scholar
  44. 44.
    Assy N, Nassar F, Nasser G, Grosovski M (2009) Olive oil consumption and non-alcoholic fatty liver disease. World J Gastroenterol 15:1809–1815CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Fraser A, Abel R, Lawlor DA, Fraser D, Elhayany A (2008) A modified Mediterranean diet is associated with the greatest reduction in alanine aminotransferase levels in obese type 2 diabetes patients: results of a quasi-randomised controlled trial. Diabetologia 51:1616–1622. doi: 10.1007/s00125-008-1049-1 CrossRefPubMedGoogle Scholar
  46. 46.
    Storniolo CE, Casillas R, Bullo M et al (2015) A Mediterranean diet supplemented with extra virgin olive oil or nuts improves endothelial markers involved in blood pressure control in hypertensive women. Eur J Nutr. doi: 10.1007/s00394-015-1060-5 PubMedGoogle Scholar

Copyright information

© Italian Society of Endocrinology (SIE) 2016

Authors and Affiliations

  • C. Santangelo
    • 1
    Email author
  • C. Filesi
    • 1
  • R. Varì
    • 1
  • B. Scazzocchio
    • 1
  • T. Filardi
    • 2
  • V. Fogliano
    • 3
  • M. D’Archivio
    • 1
  • C. Giovannini
    • 1
  • A. Lenzi
    • 2
  • S. Morano
    • 2
  • R. Masella
    • 1
  1. 1.Unit of Nutrition, Department of Veterinary Public Health and Food SafetyItalian National Institute of HealthRomeItaly
  2. 2.Department of Experimental Medicine, Section of Medical Pathophysiology, Food Science and EndocrinologySapienza University of RomeRomeItaly
  3. 3.Food Quality and Design GroupWageningen UniversityWageningenThe Netherlands

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